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Drought stress affects constitutive but not induced herbivore resistance in apple plants

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Abstract

Plant–herbivore interactions are influenced by chemical plant traits, which can vary depending on the plants’ abiotic and biotic environment. Drought events, which are predicted to become more frequent and prolonged due to climate change, may affect primary and secondary plant metabolites contributing to constitutive resistance. Furthermore, the ability of plants to respond to herbivore attack in terms of induced resistance may be altered under drought conditions. We assessed the effects of drought stress on constitutive and induced apple plant resistance to a generalist insect herbivore by quantifying plant and herbivore responses in concert. Plants were exposed to different drought stress intensities (constitutive resistance) and subsequently to herbivore damage treatments that included different damage durations (induced resistance). As drought stress intensified, plant growth and concentrations of the leaf phenolic phloridzin decreased, whereas leaf glucose concentrations increased. Changes in fructose concentrations and in herbivore feeding preferences indicated a non-monotonic shift in constitutive resistance. Moderately stressed plants showed reduced fructose concentrations and were consumed least, while severely stressed plants were fructose-enriched and consumed most compared to well-watered control plants showing intermediate fructose concentrations and palatability. We found no evidence for effects of drought stress on induced resistance, as herbivore feeding preferences for undamaged over damaged plants were independent of drought intensity. Our results suggest a strong role of primary metabolites for drought-dependent variation in constitutive plant resistance and offer novel experimental insights into the effects of drought stress on induced plant resistance across a gradient of water deprivation.

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References

  • Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432

    Article  Google Scholar 

  • Agrawal AA, Lau JA, Hamback PA (2006) Community heterogeneity and the evolution of interactions between plants and insect herbivores. Q Rev Biol 81:349–376

    Article  PubMed  Google Scholar 

  • André CM, Schafleitner R, Legay S, Lefèvre I, Aliaga CAA, Nomberto G, Hoffmann L, Hausman JF, Larondelle Y, Evers D (2009) Gene expression changes related to the production of phenolic compounds in potato tubers grown under drought stress. Phytochemistry 70:1107–1116

    Article  PubMed  Google Scholar 

  • Ballhorn DJ, Kautz S, Jensen M, Schmitt I, Heil M, Hegeman AD (2011) Genetic and environmental interactions determine plant defences against herbivores. J Ecol 99:313–326

    Article  Google Scholar 

  • Berenbaum MR (1995) Turnabout is fair play: secondary roles for primary compounds. J Chem Ecol 21:925–940

    Article  CAS  Google Scholar 

  • Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant Microbe Interact 20:1406–1420

    Article  PubMed  CAS  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought: from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Cheng LL, Zhou R, Reidel EJ, Sharkey TD, Dandekar AM (2005) Antisense inhibition of sorbitol synthesis leads to up-regulation of starch synthesis without altering CO2 assimilation in apple leaves. Planta 220:767–776

    Article  PubMed  CAS  Google Scholar 

  • Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R, Magaña Rueda V, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A, Whetton P (2007) Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change Cambridge University Press, Cambridge, pp 847–940

  • Daane KM, Williams LE (2003) Manipulating vineyard irrigation amounts to reduce insect pest damage. Ecol Appl 13:1650–1666

    Article  Google Scholar 

  • Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074

    Article  PubMed  CAS  Google Scholar 

  • Ebel RC, Mattheis JP, Buchanan DA (1995) Drought stress of apple trees alters leaf emissions of volatile compounds. Physiol Plant 93:709–712

    Article  CAS  Google Scholar 

  • English-Loeb G (1990) Plant drought stress and outbreaks of spider mites: a field test. Ecology 71:1401–1411

    Article  Google Scholar 

  • English-Loeb G, Stout MJ, Duffey SS (1997) Drought stress in tomatoes: changes in plant chemistry and potential nonlinear consequences for insect herbivores. Oikos 79:456–468

    Article  Google Scholar 

  • Frei A, Gu HN, Bueno JM, Cardona C, Dorn S (2003) Antixenosis and antibiosis of common beans to Thrips palmi Karny (Thysanoptera: Thripidae). J Econ Entomol 96:1577–1584

    Article  PubMed  Google Scholar 

  • Fulcher AF, Ranney TG, Burton JD, Walgenbach JF, Danehower DA (1998) Role of foliar phenolics in host plant resistance of Malus taxa to adult Japanese beetles. Hortscience 33:862–865

    CAS  Google Scholar 

  • Gosch C, Halbwirth H, Kuhn J, Miosic S, Stich K (2009) Biosynthesis of phloridzin in apple (Malus domestica Borkh.). Plant Sci 176:223–231

    Article  CAS  Google Scholar 

  • Gurr GM, Kvedaras OL (2010) Synergizing biological control: scope for sterile insect technique, induced plant defences and cultural techniques to enhance natural enemy impact. Biol Control 52:198–207

    Article  Google Scholar 

  • Gutbrodt B, Mody K, Dorn S (2011a) Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores. Oikos 120:1732–1740

    Article  CAS  Google Scholar 

  • Gutbrodt B, Mody K, Wittwer R, Dorn S (2011b) Within-plant distribution of induced resistance in apple seedlings: rapid acropetal and delayed basipetal responses. Planta 233:1199–1207

    Article  PubMed  CAS  Google Scholar 

  • Hale BK, Herms DA, Hansen RC, Clausen TP, Arnold D (2005) Effects of drought stress and nutrient availability on dry matter allocation, phenolic glycosides, and rapid induced resistance of poplar to two lymantriid defoliators. J Chem Ecol 31:2601–2620

    Article  PubMed  CAS  Google Scholar 

  • Halpern SL, Adler LS, Wink M (2010) Leaf herbivory and drought stress affect floral attractive and defensive traits in Nicotiana quadrivalvis. Oecologia 163:961–971

    Article  PubMed  Google Scholar 

  • Haugen R, Steffes L, Wolf J, Brown P, Matzner S, Siemens DH (2008) Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching. Oikos 117:231–244

    Article  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    Article  PubMed  CAS  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  PubMed  CAS  Google Scholar 

  • Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85:1383–1398

    Article  Google Scholar 

  • Isono K, Morita H (2010) Molecular and cellular designs of insect taste receptor system. Front Cell Neurosci 4:1–16

    Google Scholar 

  • Kanaga MK, LC Latta IV, Mock KE, Ryel RJ, Lindroth RL, Pfrender ME (2009) Plant genotypic diversity and environmental stress interact to negatively affect arthropod community diversity. Arthropod Plant Interact 3:249–258

    Article  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago

    Google Scholar 

  • Kessler A, Heil M (2011) The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357

    Article  Google Scholar 

  • Koo AJK, Howe GA (2009) The wound hormone jasmonate. Phytochemistry 70:1571–1580

    Article  PubMed  CAS  Google Scholar 

  • Li TH, Li SH (2005) Leaf responses of micropropagated apple plants to water stress: nonstructural carbohydrate composition and regulatory role of metabolic enzymes. Tree Physiol 25:495–504

    Article  PubMed  CAS  Google Scholar 

  • Lombardero MJ, Ayres MP, Lorio PL, Ruel JJ (2000) Environmental effects on constitutive and inducible resin defences of Pinus taeda. Ecol Lett 3:329–339

    Article  Google Scholar 

  • Massad TJ, Dyer LA (2010) A meta-analysis of the effects of global environmental change on plant-herbivore interactions. Arthropod Plant Interact 4:181–188

    Article  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  PubMed  Google Scholar 

  • Metlen KL, Aschehoug ET, Callaway RM (2009) Plant behavioural ecology: dynamic plasticity in secondary metabolites. Plant Cell Environ 32:641–653

    Article  PubMed  CAS  Google Scholar 

  • Mody K, Eichenberger D, Dorn S (2009) Stress magnitude matters: different intensities of pulsed water stress produce non-monotonic resistance responses of host plants to insect herbivores. Ecol Entomol 34:133–143

    Article  Google Scholar 

  • Mody K, Spoerndli C, Dorn S (2011) Within-orchard variability of the ecosystem service ‘parasitism’: effects of cultivars, ants and tree location. Basic Appl Ecol 12:456–465

    Article  Google Scholar 

  • Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268

    Article  Google Scholar 

  • Olson DM, Cortesero AM, Rains GC, Potter T, Lewis WJ (2009) Nitrogen and water affect direct and indirect plant systemic induced defense in cotton. Biol Control 49:239–244

    Article  CAS  Google Scholar 

  • Plath M, Mody K, Potvin C, Dorn S (2011) Establishment of native tropical timber trees in monoculture and mixed-species plantations: small-scale effects on tree performance and insect herbivory. For Ecol Manag 261:741–750

    Article  Google Scholar 

  • Plath M, Dorn S, Riedel J, Barrios H, Mody K (2012) Associational resistance and associational susceptibility: specialist herbivores show opposite responses to tree stand diversification. Oecologia. doi:10.1007/s00442-011-2215-6

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Article  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54

    Google Scholar 

  • Salama HS, Dimetry NZ, Salem SA (1970) On the host preference and biology of the cotton leaf worm Spodoptera littoralis. J Appl Entomol 67:261–266

    Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, New York

    Google Scholar 

  • Showler AT, Moran PJ (2003) Effects of drought stressed cotton, Gossypium hirsutum L., on beet armyworm, Spodoptera exigua (Hubner), oviposition, and larval feeding preferences and growth. J Chem Ecol 29:1997–2011

    Article  PubMed  CAS  Google Scholar 

  • Sircelj H, Tausz M, Grill D, Batic F (2005) Biochemical responses in leaves of two apple tree cultivars subjected to progressing drought. J Plant Physiol 162:1308–1318

    Article  PubMed  CAS  Google Scholar 

  • Smith CM, Clement SL (2012) Molecular bases of plant resistance to arthropods. Annu Rev Entomol 57:309–328

    Google Scholar 

  • Stoeckli S, Mody K, Dorn S (2008) Aphis pomi (Hemiptera: Aphididae) population development, shoot characteristics, and antibiosis resistance in different apple genotypes. J Econ Entomol 101:1341–1348

    Article  PubMed  Google Scholar 

  • Stout MJ (2007) Types and mechanisms of rapidly induced plant resistance to herbivorous arthropods. In: Walters D, Newton A, Lyon G (eds) Induced resistance for plant defense: a sustainable approach to crop protection. Blackwell Publishing, Oxford, pp 89–107

    Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285

    Article  Google Scholar 

  • Turtola S, Manninen AM, Rikala R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. J Chem Ecol 29:1981–1995

    Article  PubMed  CAS  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  PubMed  Google Scholar 

  • Vallat A, Dorn S (2005) Changes in volatile emissions from apple trees and associated response of adult female codling moths over the fruit-growing season. J Agric Food Chem 53:4083–4090

    Article  PubMed  CAS  Google Scholar 

  • Vallat A, Gu HN, Dorn S (2005) How rainfall, relative humidity and temperature influence volatile emissions from apple trees in situ. Phytochemistry 66:1540–1550

    Article  PubMed  CAS  Google Scholar 

  • White TCR (1969) An index to measure weather-induced stress of trees associated with outbreaks of psyllids in Australia. Ecology 50:905–909

    Article  Google Scholar 

  • White TCR (2009) Plant vigour versus plant stress: a false dichotomy. Oikos 118:807–808

    Article  Google Scholar 

  • Wu JQ, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24

    Article  PubMed  CAS  Google Scholar 

  • Yule KM, Woolley JB, Rudgers JA (2011) Water availability alters the tri-trophic consequences of a plant-fungal symbiosis. Arthropod Plant Interact 5:19–27

    Article  Google Scholar 

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Acknowledgments

We thank Rafal Piskorski, Andreas Bühler and Laura Nyström for useful support in chemical analyses, Roland Reist (Syngenta Switzerland) for providing test insects, Anna Drewek for statistical advice and Jana Collatz for constructive comments on the manuscript.

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Authors and Affiliations

  1. Institute of Agricultural Sciences, Applied Entomology, ETH Zurich, Schmelzbergstrasse 9/LFO, 8092, Zurich, Switzerland

    Bettina Gutbrodt, Silvia Dorn & Karsten Mody

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  1. Bettina Gutbrodt
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  2. Silvia Dorn
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  3. Karsten Mody
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Correspondence to Karsten Mody.

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Handling editor: Gary Felton.

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Gutbrodt, B., Dorn, S. & Mody, K. Drought stress affects constitutive but not induced herbivore resistance in apple plants. Arthropod-Plant Interactions 6, 171–179 (2012). https://doi.org/10.1007/s11829-011-9173-0

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  • DOI: https://doi.org/10.1007/s11829-011-9173-0

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